The macaque oocyte is the intragonadal site of a functional dopaminergic system capable of dopamine (DA) uptake and norepinephrine synthesis. RT-PCR with primers complementary to highly conserved regions of the rat and human dopamine-beta-hydroxylase (DBH) gene and cumulus-free oocyte mRNA as a template yielded a cDNA encoding a mRNA identical in size and sequence to adrenal DBH. In situ hybridization identified oocytes as the major site of DBH expression in the ovary. This expression was located in oocytes of pre-antral, small, medium and large antral follicles. Both conventional and confocal microscopy, coupled with immunohistochemical analysis for the DBH protein, identified oocytes as expressing the DBH mRNA protein-product. The oocyte does not contain TH mRNA but does express a DA transporter gene. Next, cumulus and corona cells were removed from GV oocytes which were then cultured in the presence or absence of DA. The media was collected and assayed for NE. The results indicate that the oocyte is capable of DA uptake and that the DBH enzyme is active and can convert DA to NE. We then conducted experiments investigating the interaction of the follicle and the oocyte with respect to this dopaminergic system and a possible role in regulating intrafollicular cAMP levels. Culture of oocyte intact follicles for 9 hr in the presence of DA results in elevated cAMP production compared to controls (-DA) and follicles without oocytes. Addition of propranolol, a -adrenergic receptor blocker, nullified the stimulatory influence of DA on cAMP production from oocyte-intact follicles. This suggests a novel cell-cell communication system involving the oocyte, follicular cells, an oocyte dopaminergic system, NE production and cAMP. In the follicle, this system may be involved with folliculogenesis (recruitment, dominance, atresia and apoptosis), steroidogenesis, and/or maintenance of oocyte meiotic arrest.